Combined use of two supervised learning algorithms to model sea turtle behaviours from tri-axial acceleration data.

Accelerometers are becoming ever more important sensors in animal-attached technology, providing data that allow determination of body posture and movement and thereby helping to elucidate behaviour in animals that are difficult to observe. We sought to validate the identification of sea turtle behaviours from accelerometer signals by deploying tags on the carapace of a juvenile loggerhead (Caretta caretta), an adult hawksbill (Eretmochelys imbricata) and an adult green turtle (Chelonia mydas) at Aquarium La Rochelle, France. We recorded tri-axial acceleration at 50 Hz for each species for a full day while two fixed cameras recorded their behaviours. We identified behaviours from the acceleration data using two different supervised learning algorithms, Random Forest and Classification And Regression Tree (CART), treating the data from the adult animals as separate from the juvenile data. We achieved a global accuracy of 81.30% for the adult hawksbill and green turtle CART model and 71.63% for the juvenile loggerhead, identifying 10 and 12 different behaviours, respectively. Equivalent figures were 86.96% for the adult hawksbill and green turtle Random Forest model and 79.49% for the juvenile loggerhead, for the same behaviours. The use of Random Forest combined with CART algorithms allowed us to understand the decision rules implicated in behaviour discrimination, and thus remove or group together some 'confused' or under--represented behaviours in order to get the most accurate models. This study is the first to validate accelerometer data to identify turtle behaviours and the approach can now be tested on other captive sea turtle species.

Emperor penguin body surfaces cool below air temperature.

Emperor penguins Aptenodytes forsteri are able to survive the harsh Antarctic climate because of specialized anatomical, physiological and behavioural adaptations for minimizing heat loss. Heat transfer theory predicts that metabolic heat loss in this species will mostly depend on radiative and convective cooling. To examine this, thermal imaging of emperor penguins was undertaken at the breeding colony of Pointe Géologie in Terre Adélie (66°40' S 140° 01' E), Antarctica in June 2008. During clear sky conditions, most outer surfaces of the body were colder than surrounding sub-zero air owing to radiative cooling. In these conditions, the feather surface will paradoxically gain heat by convection from surrounding air. However, owing to the low thermal conductivity of plumage any heat transfer to the skin surface will be negligible. Future thermal imaging studies are likely to yield further insights into the adaptations of this species to the Antarctic climate.

Influence of weather conditions on the flight of migrating black storks.

This study tested the potential influence of meteorological parameters (temperature, humidity, wind direction, thermal convection) on different migration characteristics (namely flight speed, altitude and direction and daily distance) in 16 black storks (Ciconia nigra). The birds were tracked by satellite during their entire autumnal and spring migration, from 1998 to 2006. Our data reveal that during their 27-day-long migration between Europe and Africa (mean distance of 4100 km), the periods of maximum flight activity corresponded to periods of maximum thermal energy, underlining the importance of atmospheric thermal convection in the migratory flight of the black stork. In some cases, tailwind was recorded at the same altitude and position as the birds, and was associated with a significant rise in flight speed, but wind often produced a side azimuth along the birds' migratory route. Whatever the season, the distance travelled daily was on average shorter in Europe than in Africa, with values of 200 and 270 km d(-1), respectively. The fastest instantaneous flight speeds of up to 112 km h(-1) were also observed above Africa. This observation confirms the hypothesis of thermal-dependant flight behaviour, and also reveals differences in flight costs between Europe and Africa. Furthermore, differences in food availability, a crucial factor for black storks during their flight between Europe and Africa, may also contribute to the above-mentioned shift in daily flight speeds.

Ecophysiological response of Adelie penguins facing an experimental increase in breeding constraints.

Foraging strategies play a key role in breeding effort. Little is known, however, about their connection with hormonal and nutritional states, especially when breeding constraints vary. Here, we experimentally increased foraging costs and thus breeding constraints by handicapping Adélie penguins (Pygoscelis adeliae) with dummy devices representing 3-4% of the penguins' cross-sectional area. We examined food-related stress (via plasma corticosterone concentration) and nutritional state (via metabolite levels). Concurrently, we investigated the use of ecological niches via the isotopic signature of red blood cells indicating the trophic position (delta(15)N) and the spatial distribution (delta(13)C) of penguins. Handicapped birds performed approximately 70% longer foraging trips and lost approximately 60% more body mass than controls and their partners. However, corticosterone levels and the nutritional state were unchanged. The isotopic signature revealed that males and females differed in their foraging behaviour: upper trophic levels contributed more in the males' diet, who foraged in more pelagic areas. Handicapped and partner birds adopted the same strategy at sea: a shift towards higher delta(13)C values suggested that they foraged in more coastal areas than controls. This change in foraging decisions may optimize feeding time by decreasing travelling time. This may partly compensate for the presumed lower foraging efficiency of handicapped birds and for the energetic debt of their partners who had to fast approximately 70% longer on the nest. We propose that this flexible use of ecological niches may allow birds facing increased breeding constraints to avoid chronic stress and to minimize the impact on their body condition.

Effect of fasting and thyroidectomy on cysteine proteinase activities in liver and muscle.

Prolonged starvation mimics chronic negative nitrogen balance observed in many physiopathological situations. During starvation, an initial decrease in protein utilization (phase I) is followed by a long period of protein sparing (phase II) that ends with a marked rise in nitrogen excretion (phase III). Variations in protein metabolism during starvation are determined by changes in protein synthesis and degradation rates (Cherel, Y., Attaix, D. Rosolowska-Huszcz, D., Belkhou, R., Robin, J.P., Arnal, M. and Le Maho, Y. (1991) Clin. Sci. 81, 611-619), but little information is available on expression of proteolytic systems. In this study, cathepsin B, H and L activities were compared in hindlimb muscles and liver at various phases of starvation in thyroidectomized and sham-operated rats. In muscle, cathepsin activities fell from the fed state to phase II, which suggests that cathepsins may play a role in the curtailment of muscle proteolysis during protein sparing phase. This decrease of muscle cathepsin activities was reproduced by thyroidectomy alone. In contrast, liver cathepsin B and H activities fell during starvation, but were not affected by thyroidectomy alone. Liver cathepsin L decreased only during starvation in thyroidectomized animals. These observations emphasize that different mechanisms modulate cathepsin expression in skeletal muscle and liver.

Feeding behaviour of free-ranging penguins determined by oesophageal temperature.

Sea birds play a major role in marine food webs, and it is important to determine when and how much they feed at sea. A major advance has been made by using the drop in stomach temperature after ingestion of ectothermic prey. This method is less sensitive when birds eat small prey or when the stomach is full. Moreover, in diving birds, independently of food ingestion, there are fluctuations in the lower abdominal temperature during the dives. Using oesophageal temperature, we present here a new method for detecting the timing of prey ingestion in free-ranging sea birds, and, to our knowledge, report the first data obtained on king penguins (Aptenodytes patagonicus). In birds ashore, which were hand-fed 2-15 g pieces of fish, all meal ingestions were detected with a sensor in the upper oesophagus. Detection was poorer with sensors at increasing distances from the beak. At sea, slow temperature drops in the upper oesophagus and stomach characterized a diving effect per se. For the upper oesophagus only, abrupt temperature variations were superimposed, therefore indicating prey ingestions. We determined the depths at which these occurred. Combining the changes in oesophageal temperatures of marine predators with their diving pattern opens new perspectives for understanding their foraging strategy, and, after validation with concurrent applications of classical techniques of prey survey, for assessing the distribution of their prey.

Long-term effects of flipper bands on penguins.

Changes in seabird populations, and particularly of penguins, offer a unique opportunity for investigating the impact of fisheries and climatic variations on marine resources. Such investigations often require large-scale banding to identify individual birds, but the significance of the data relies on the assumption that no bias is introduced in this type of long-term monitoring. After 5 years of using an automated system of identification of king penguins implanted with electronic tags (100 adult king penguins were implanted with a transponder tag, 50 of which were also flipper banded), we can report that banding results in later arrival at the colony for courtship in some years, lower breeding probability and lower chick production. We also found that the survival rate of unbanded, electronically tagged king penguin chicks after 2-3 years is approximately twice as large as that reported in the literature for banded chicks.

In vivo glucose utilization in rat tissues during the three phases of starvation.

Three phases of starvation have been described from changes in protein and lipid utilization in birds and mammals. In the present study, tissue glucose utilization was measured in vivo during these three phases, using a 2-deoxy-[1-3H]glucose technique in the anesthetized rat. According to this technique, the term glucose utilization therefore refers to transport and phosphorylation of glucose in tissues, ie, whatever is the fate of glucose. Whole-body glucose turnover rate, which was determined by a continuous infusion of [3-3H]glucose, decreased by 40% during the first two days of starvation (phase 1); it did not change thereafter, neither in the protein-sparing phase 2 nor in phase 3, which is marked by an increase in net protein breakdown. Two days of starvation caused a marked decrease in the glucose utilization in skeletal muscles; this decrease was higher in oxidative muscles (65% in diaphragm, 66% in soleus) than in glycolytic muscles (31% in extensor digitorum longus, 34% in epitrochlearis). Glucose utilization also decreased in heart atria (75%), heart ventricles (93%), and white adipose tissue (54%); by contrast, there was a two-fold increase in glucose utilization in brown adipose tissue and no change in brain and skin. No variations were observed in glucose utilization in any of the tissues from phase 1 to phase 2. However, phase 3 was marked by a decrease in glucose utilization in extensor digitorum longus (45%), brown adipose tissue (76%), brain (29%), and skin (40%), whereas there was a 2.3- and 3.4-fold increase in glucose utilization in diaphragm and heart ventricles, respectively.(ABSTRACT TRUNCATED AT 250 WORDS)

Ventromedial hypothalamic lesions prevent the fasting-induced changes in day-night pattern of locomotor activity.

The time-course of day-night organization of running wheel activity during prolonged fasting was studied in rats, with or without electrolytic lesions in the ventromedial hypothalamus (VMH). For each individual, dates were referenced to the metabolic transition from lipid to protein utilization in late fasting; this was estimated by daily weighing. In fasted sham-operated controls, daytime activity increased progressively over the fast. This fasting-induced rise in diurnal activity was not due to daily handling, since it was observed also in non-handled (fasted) controls. The pattern of the increase in sham-operated rats differed between 2-hour periods (8-10 h to 18-20 h). The distribution of nocturnal activity was also modified during food deprivation: nocturnal activity in late fasting increased in the 20-22 h period and concomitantly decreased in the two 4-6 h and 6-8 h periods. By contrast, VMH lesions markedly limited and delayed the rise in diurnal running activity, irrespective of the 2-hour period. They prevented any significant change in nocturnal activity pattern over the fast. In fasted sham-operated rats, the data may be interpreted as a phase-advance of the nocturnal pattern of locomotor activity, concomitant with the increase of activity during daytime. These changes were suppressed by the VMH lesions. This suggests that the fasting-induced changes in the day-night pattern of locomotor activity are centrally mediated by a neuronal circuit involving the ventromedial hypothalamus.

Refeeding after the late increase in nitrogen excretion during prolonged fasting in the rat.

Recovery of body mass, food intake and body composition was studied in the laboratory rat after the late increase in nitrogen excretion that characterizes prolonged fasting in mammals and birds. The rats lost 43% of their body mass during 13 days of food deprivation. They all regained their prefasting body mass within a shorter period of 11 days of refeeding. These results confirm that the late increase in nitrogen excretion in rats, as in spontaneously fasting birds, is reversible and is a part of the physiological adaptations to long-term food deprivation. Water intake of the rats continuously decreased during fasting, and the animals virtually stopped drinking as protein utilization increased. On refeeding, changes in water intake paralleled those in food intake. The refed rats progressively increased their daily food intake, that was always higher than the prefasting value (8.0-10.4 vs. 6.7% of body mass). The comparison of organ weights between fed and ad lib refed rats of similar body weight indicates that muscle mass was regained earlier than body fat during refeeding. The laboratory rat therefore appears to be a good experimental model to investigate the metabolic and behavioural changes that occur during spontaneous anorexia and refeeding in wild animals.

Locomotor activity and utilization of energy reserves during fasting after ventromedial hypothalamic lesions.

The ventromedial hypothalamus (VMH) is known to be involved in the regulation of energy metabolism but it may also modulate locomotor activity. Since prolonged fasting is marked by a succession of changes in energy utilization and locomotor activity, it was hypothesized that VMH may be a critical link controlling mobilization of energy stores and/or behavioral changes in response to fasting. To test this, the changes in rate of body mass loss, body content in lipid and protein, and wheel-running activity were studied in fasted nonobese rats with VMH electrolytic lesions. Secondary effects of VMH obesity were ruled out by postoperative restricted feeding. During fasting, VMH lesions impaired neither the overall lipid mobilization nor the late rise in daily body mass loss, concomitant with the increase in net proteolysis. Despite that the onset of this late stage of fasting was significantly delayed in VMH vs. sham-operated rats (13 +/- 1 vs. 8 +/- 1 days, respectively), the final amount of reserve lipids (3 g) was closely similar in both groups: this is the first experimental evidence of the hypothesis of a lipidic set-point. These results indicate that VMH is not a critical link controlling the time-course of utilization of energy reserves. The increase in diurnal (and total) daily wheel-running observed in fasted sham-operated rats still occurred in fasted VMH rats but was significantly reduced and delayed. VMH nuclei and/or associated fibers are therefore involved in the fasting-induced rise in diurnal activity.

Refeeding in fasted rats: dietary self-selection according to metabolic status.

We investigated the influence of the metabolic status rats have reached during a fast on their selection of protein, fat and carbohydrate when allowed to refeed after fasting for different lengths of time. They were refed either while essentially relying on lipid fuels (group 1), or while in the further stage when there is a rise in protein breakdown (group 2). In contrast to previous studies in which rats could not select macronutrients, there was no transitory anorexia during refeeding. Macronutrient selection as well as food and energy intake on the first day of refeeding were the same for both groups, total food intake being significantly larger than prior to the fast. However, there was thereafter a distinct pattern of diet selection: while fat intake progressively decreased in group 1, it increased until the fifth day in rats of groups 2. These rats, moreover, exhibited a further rise in protein intake. The data are discussed in relation to the optimization of the restoration of body fuel reserves according to the metabolic status reached at the end of a long fast.

An electrophysiological and behavioral study of sleep in emperor penguins under natural ambient conditions.

In two pairs of emperor penguins surgically implanted for chronic recordings of EEG, EOG and EMG, four arousal stages were characterized on the basis of behavioral and electrophysiological criteria: wakefulness (W), drowsiness (D), slow-wave sleep (SWS) and paradoxical sleep (PS). The general patterns of electrographic correlates observed for each arousal stage resemble those reported in other birds. Sleep patterns were examined with these two pairs placed under natural ambient conditions of light and air temperature, the first pair being exposed to moderate cold under alternate conditions of day and night, and the second studied when daylight was total at thermoneutrality. The time spent in sleep (TST) by each group was 41.3% and 45.1% of the 24 hr period respectively, the difference not being significant. As in other birds, PS occurred in very brief episodes lasting, on average, 8 to 10 seconds and occupying only 5 to 6% of the 24 hr period. Whatever the external conditions, the PS to TST ratio appeared to remain unchanged (12 to 14%). Its relatively high value is discussed in relation to predation susceptibility.

Polygraphic and behavioral study of sleep in geese: existence of nuchal atonia during paradoxical sleep.

In adult geese, chronic polygraphic recordings of EEG, EOG, EMG, ECG and respiratory rate completed with behavioral observations allowed the characterization of four states of vigilance: wakefulness (W), drowsiness (D), slow wave sleep (SWS) and paradoxical sleep (PS). The EEG, EOG, EMG general patterns observed during W, D, SWS and PS episodes with nuchal isotonia or hypotonia were similar to those reported in other birds. The characteristic brevity of avian PS was confirmed since this sleep state occupied only 2.8% of the nycthemere in geese. For the first time in an adult bird it was shown that numerous PS episodes were accompanied, as in mammals, by a total disappearance of nuchal EMG activity. These observations made in a bird species with a stable head support when sleeping, suggest that, as in mammals, inhibitory mechanisms leading to a PS related nuchal atonia do exist and that head falling is not the cause of PS episodes brevity in birds.

Fasting-induced rise in locomotor activity in rats coincides with increased protein utilization.

The aim of this study was to investigate the possible relation between the modifications in locomotor activity (on running wheel) which occur during prolonged fasting and changes in the utilization of energy reserves. In 18-week-old rats, we found that the rate of body mass loss reflects the changes in nitrogen excretion that occur over three phases of fasting: (I) initially decreasing, (II) maintained at a low level and (III) increasing. Locomotor activity started to increase during phase II without a change in its nycthemeral pattern. By contrast, the 10-fold higher daily locomotor activity that occurred in phase III was marked by a higher proportion of diurnal activity. Using 9-, 18-, and 33-week-old rats, in order to obtain a different timing in the metabolic changes during fasting, we could confirm the coincidence between the later rise in locomotor activity and the occurrence of phase III. Refeeding of rats of either age in phase III rapidly suppressed fasting-induced changes in locomotor activity. These data accord with the idea that behavioral changes reflecting the search for food are triggered by a later and reversible change in the utilization of body protein vs. lipid stores during prolonged fasting.

Foraging strategies of incubating and brooding king penguins Aptenodytes patagonicus.

For oceanic birds like king penguins, a major constraint is the separation of foraging areas from the breeding colony, largely because swimming increases foraging costs. However, the relationship between foraging strategy and breeding stage has been poorly investigated. Using time-depth recorders, we studied the diving behaviour of two groups of king penguins that were either incubating or brooding chicks at Crozet Islands (Southern Indian Ocean) at the same period of the year. Although birds with chicks had the highest predicted energy demand, they made foraging trips half as long as incubating birds (6 vs. 14 days) and modified their time and depth utilisation. Birds with chicks dived deeper during daylight (mean maximum depth of 280 m vs. 205 m for those incubating). At night, birds with chicks spent twice as much time diving as those incubating, but birds at both stages never dived beyond 30 m. Movements to greater depths by brooding birds are consistent with the vertical distribution of myctophid fish which are the main prey. As chick provisioning limits trip duration, it is suggested that it is more efficient for parents to change their diving patterns rather than to restrict their foraging range.

Involvement of corticosterone in the fasting-induced rise in protein utilization and locomotor activity.

During fasting, most of the energy is derived from lipids whereas proteins are efficiently spared. However, there is a late rise in net protein utilization. Fasting is also associated with an increase in locomotor activity. Because the plasma corticosterone level increases concomitantly with these metabolic and behavioral changes, the involvement of corticosterone has been hypothesized. To test this, the net protein utilization and locomotor activity were investigated in fasted adrenalectomized (Adx) rats, with or without replacement with corticosterone, and in fasted intact rats treated with RU486, an antagonist of type II glucocorticoid receptors. During the phase of fasting characterized by protein sparing, urine nitrogen loss was further reduced in Adx rats and in RU486-treated controls compared with intact rats and with Adx rats with corticosterone replacement: this indicates a catabolic effect of corticosterone through type II receptors. In the last phase of fasting, the rise in net protein breakdown was suppressed in Adx rats and restored by corticosterone replacement. The increase in locomotor activity induced by fasting in controls was suppressed in Adx and restored by corticosterone replacement. This rise in running activity was still present in RU486-treated rats. In conclusion, this study shows that corticosterone plays a critical role in the changes of both protein catabolism and locomotor activity during prolonged fasting.

Impact of externally attached loggers on the diving behaviour of the king penguin.

The impact of relatively small externally attached time series recorders on some foraging parameters of seabirds was investigated during the austral summer of 1995 by monitoring the diving behaviour of 10 free-ranging king penguins (Aptenodytes patagonicus) over one foraging trip. Time-depth recorders were implanted in the abdominal cavities of the birds, and half of the animals also had dummy loggers attached on their backs. Although most of the diving behaviour was not significantly affected by the external loggers (P>0.05), the birds with externally attached loggers performed almost twice as many shallow dives, between 0 and 10 m depth, as the birds without external loggers. These shallow dives interrupted more frequently the deep-diving sequences in the case of birds with external loggers (percentage of deep dives followed by deep dives: 46% for birds with implants only vs. 26% for birds with an external attachment). Finally, the distribution pattern of the postdive durations plotted against the hour of the day was more heterogeneous for the birds with an external package. In addition, these penguins had extended surfacing times between two deep dives compared to birds without external attachments (P<0.0001). These results suggest the existence of an extra energy cost induced by externally attached loggers.

[Metabolic adaptations to prolonged fasting in birds]. / Adaptations métaboliques au jeûne prolongé chez l'oiseau.

Because they tolerate remarkably long periods of fasting, birds appear as interesting models to study the mechanisms for decreasing metabolic rate and sparing proteins. In particular, the comprehension of the metabolic changes occurring during the three periods of fasting which have been characterized, might be helpful for determining the possible role of ketone bodies in the adaptation to long-term fasting.